Evidence for pleistocene population divergence and expansion of Anopheles albimanus in Southern Central America.

The micro-geographic structure of Anopheles albimanus was studied in southern Central America using partial sequences of the mtDNA cytochrome oxidase subunit I gene (COI). Analysis of molecular variance supported significant genetic structure between populations from Costa Rica and western Panama versus those from central-eastern Panama (Phi(CT) = 0.33), whereas the within group divergence was shallow and statistically insignificant (Phi(ST) = 0.08). Furthermore, a statistical parsimony network depicted three divergent groups of haplotypes that were not evenly distributed across the study area. Our findings are in partial agreement with previous studies, yet they do not support physical barriers to gene flow or contemporary isolation by distance in this region. Instead, three co-occurring groups of An. albimanus may be the result of multiple introductions, most likely caused by historical fragmentation and subsequent secondary contact. In addition, the molecular signature of population expansion of An. albimanus was detected in central-eastern Panama approximately 22,000 years ago (95% confidence interval [CI] 10,183-38,169). We hypothesize that the population structure of An. albimanus, as determined by our COI locus analysis, is the result of late Pleistocene climatic changes in northern South America.

[1]  E. Bermingham,et al.  Anopheles darlingi (Diptera: Culicidae) in Panama. , 2009, The American journal of tropical medicine and hygiene.

[2]  H. Kishino,et al.  Complex population history of two Anopheles dirus mosquito species in Southeast Asia suggests the influence of Pleistocene climate change rather than human‐mediated effects , 2008, Journal of evolutionary biology.

[3]  E. Bermingham,et al.  Species Composition and Distribution of Adult Anopheles (Diptera: Culicidae) in Panama , 2008, Journal of medical entomology.

[4]  E. Bermingham,et al.  Species Composition and Distribution of AdultAnopheles(Diptera: Culicidae) in Panama , 2008 .

[5]  J. Pascale,et al.  Revising antimalarial drug policy in Central America: experience in Panama. , 2008, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[6]  L. Mirabello,et al.  Population analysis using the nuclear white gene detects Pliocene/Pleistocene lineage divergence within Anopheles nuneztovari in South America , 2008, Medical and veterinary entomology.

[7]  R. Zink,et al.  Mitochondrial DNA under siege in avian phylogeography , 2008, Molecular ecology.

[8]  Lisa Mirabello,et al.  Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America , 2008, BMC Ecology.

[9]  L. Mirabello,et al.  The biogeography and population genetics of neotropical vector species , 2007, Heredity.

[10]  E. Rejmánková,et al.  A MARK–RELEASE–RECAPTURE STUDY TO DEFINE THE FLIGHT BEHAVIORS OF ANOPHELES VESTITIPENNIS AND ANOPHELES ALBIMANUS IN BELIZE, CENTRAL AMERICA1 , 2007, Journal of the American Mosquito Control Association.

[11]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[12]  J. Conn,et al.  Population genetic structure of the major malaria vector Anopheles darlingi (Diptera: Culicidae) from the Brazilian Amazon, using microsatellite markers. , 2007, Memorias do Instituto Oswaldo Cruz.

[13]  M. Milinkovitch,et al.  Estimating population parameters using the structured serial coalescent with Bayesian MCMC inference when some demes are hidden. , 2007 .

[14]  L. Mirabello,et al.  Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America , 2006, Heredity.

[15]  José Ignacio Manteca Martínez,et al.  Late Quaternary vegetation and climate change in the Panama Basin: Palynological evidence from marine cores ODP 677B and TR 163-38 , 2006 .

[16]  Jonathan P. Bollback,et al.  Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. , 2006, The American journal of tropical medicine and hygiene.

[17]  J. Diniz‐Filho,et al.  Multiple Mantel tests and isolation-by-distance, taking into account long-term historical divergence. , 2005, Genetics and molecular research : GMR.

[18]  M. Ryan,et al.  Biogeography of the túngara frog, Physalaemus pustulosus: a molecular perspective , 2005, Molecular ecology.

[19]  J. Grieco,et al.  COMPARATIVE SUSCEPTIBILITY OF THREE SPECIES OF ANOPHELES FROM BELIZE, CENTRAL AMERICA, TO PLASMODIUM FALCIPARUM (NF-54) , 2005, Journal of the American Mosquito Control Association.

[20]  S. Kelley,et al.  Isolation by distance, web service , 2005, BMC Genetics.

[21]  S. Schneider,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[22]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[23]  J. Losos,et al.  Genetic variation increases during biological invasion by a Cuban lizard , 2004, Nature.

[24]  W. Black,et al.  Gene flow among Anopheles albimanus populations in Central America, South America, and the Caribbean assessed by microsatellites and mitochondrial DNA. , 2004, The American journal of tropical medicine and hygiene.

[25]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[26]  D. W. Zeh,et al.  Phylogeography of the harlequin beetle‐riding pseudoscorpion and the rise of the Isthmus of Panamá , 2003, Molecular ecology.

[27]  J. Benzie,et al.  Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo‐Pacific , 2003, Molecular ecology.

[28]  W. Hawley,et al.  Population Structure of Anopheles gambiae in Africa. , 2003, The Journal of heredity.

[29]  J. Rozas,et al.  Statistical properties of new neutrality tests against population growth. , 2002, Molecular biology and evolution.

[30]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[31]  J. Conn,et al.  Effects of Local Geographic Barriers and Latitude on Population Structure in Anopheles punctipennis (Diptera: Culicidae) , 2000, Journal of medical entomology.

[32]  R. Butlin,et al.  Population structure and population history of Anopheles dirus mosquitoes in Southeast Asia. , 2000, Molecular biology and evolution.

[33]  K. Crandall,et al.  GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes , 2000, Molecular ecology.

[34]  W. Black,et al.  Mitochondrial DNA variation among Anopheles albimanus populations. , 1999, The American journal of tropical medicine and hygiene.

[35]  A. Cockburn,et al.  MITOCHONDRIAL DNA ANALYSIS OF THE NEOTROPICAL MALARIA VECTOR ANOPHELES NUNEZTOVARI , 1998 .

[36]  Andrew P. Martin,et al.  Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America , 1998, Molecular ecology.

[37]  Templeton,et al.  Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history , 1998, Molecular ecology.

[38]  Y. Fu,et al.  Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. , 1997, Genetics.

[39]  D. Lunt,et al.  The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies , 1996, Insect molecular biology.

[40]  W. Black,et al.  Variation in ribosomal DNA intergenic spacers among populations of Anopheles albimanus in South and Central America. , 1995, The American journal of tropical medicine and hygiene.

[41]  A. Rogers.  GENETIC EVIDENCE FOR A PLEISTOCENE POPULATION EXPLOSION , 1995, Evolution; international journal of organic evolution.

[42]  A. Templeton,et al.  Root probabilities for intraspecific gene trees under neutral coalescent theory. , 1994, Molecular phylogenetics and evolution.

[43]  E. Frederickson.  Bionomics and Control of Anopheles Albimanus , 1993 .

[44]  Stephen T. Sherry,et al.  The Genetic Structure of Ancient Human Populations , 1993, Current Anthropology.

[45]  K. Crandall,et al.  Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. , 1993, Genetics.

[46]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[47]  W. Li,et al.  Statistical tests of neutrality of mutations. , 1993, Genetics.

[48]  Wayne P. Maddison,et al.  Macclade: Analysis of Phylogeny and Character Evolution/Version 3 , 1992 .

[49]  S. Narang,et al.  Genetic structure of natural populations of Anopheles albimanus in Colombia. , 1991, Journal of the American Mosquito Control Association.

[50]  D. Strickman,et al.  Illustrated key to the female anopheline mosquitoes of Central America and Mexico. , 1990, Journal of the American Mosquito Control Association.

[51]  F. Tajima.  Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[52]  F. Collins,et al.  Structure of Ribosomal Dna in Anopheles albimanus (Diptera: Culicidae) , 1989 .

[53]  T. Ishii,et al.  Highly polluted larval habitats of the Culex pipiens complex in central Sweden. , 1987, Journal of the American Mosquito Control Association.

[54]  M. Nei.  Molecular Evolutionary Genetics , 1987 .

[55]  J. Powell,et al.  Rates of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[56]  J. Sexton,et al.  The biting and resting behavior of Anopheles albimanus in northern Haiti. , 1986, Journal of the American Mosquito Control Association.

[57]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[58]  W. Collins,et al.  Studies on human malaria in Aotus monkeys. VII. Comparative infectivity of two strains of Plasmodium vivax to Anopheles freeborni, A. maculatus, and four strains of A. albimanus. , 1976 .

[59]  S. G. Breeland.  Studies on the ecology of Anopheles albimanus. , 1972, The American journal of tropical medicine and hygiene.

[60]  A. Golik.  History of Holocene Transgression in the Gulf of Panama , 1968, The Journal of Geology.

[61]  N. Mantel.  The detection of disease clustering and a generalized regression approach. , 1967, Cancer research.

[62]  H. Trapido.  Modified response of Anopheles albimanus to DDT residual house spraying in Panama. , 1952, The American journal of tropical medicine and hygiene.

[63]  L. Mirabello.  Molecular population genetics of the malaria vector Anopheles darlingi throughout Central and South America using mitochondrial, nuclear, and microsatellite markers , 2007 .

[64]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[65]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[66]  M. Faran.  Mosquito studies (Diptera, Cilicidae). XXXIV. A revision of the albimanus section of the subgenus Nyssorhynchus of Anopheles. , 1980 .